Interfacial Water Arrangement in the Ice-Bound State of an Antifreeze Protein: A Molecular Dynamics Simulation Study

Molecular dynamics (MD) simulations have been carried out to study the heterogeneous ice nucleation on modeled peptide surfaces. Simulations show that large peptide surfaces made by TxT (threonine-x-threonine) motifs with the arrangements of threonine (Thr) residues identical to the periodic arrangements of waters on either the basal or prism plane of ice are capable of ice nucleation. Nucleated ice plane is the (0001) basal plane of hexagonal ice (Ih) or (111) plane of cubic ice (Ic). However, due to predefined simulation cell dimensions, the ice growth is only observed on the surface where the Thr residues are arranged like the water arrangement on the basal plane of ice Ih. The γ-methyl and γ-hydroxyl groups of Thr residue are necessary for such ice formation. From this ice nucleation and growth simulation, the interfacial water arrangement in the ice-bound state of Tenebrio molitor antifreeze protein (TmAFP) has been determined. The interfacial water arrangement in the ice-bound state of TmAFP is characterized by five-membered hydrogen bonded rings, where each of the hydroxyl groups of the Thr residues on the ice-binding surface (IBS) of the protein is a ring member. It is found that the water arrangement at the protein-ice interface is distorted from that in bulk ice. Our analysis further reveals that the hydroxyl groups of Thr residues on the IBS of TmAFP form maximum three hydrogen bonds each with the waters in the bound state and methyl groups of Thr residues occupy wider spaces than the normal grooves on the (111) plane of ice Ic. Methyl groups are also located above and along the 3-fold rotational axes of the chair-formed hexagonal hydrogen bonded water rings on the (111) plane.